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Abstract

Background

The avoidance of inhaled allergens or tobacco smoke has been known to have
favorable effects on asthma control. However, it remains unclear whether
other lifestyle-related factors are also related to asthma control.
Therefore, a comprehensive study to examine the associations between various
lifestyle factors and asthma control was conducted in Japanese asthmatic
patients.

Methods

The study subjects included 437 stable asthmatic patients recruited from our
outpatient clinic over a one-year period. A written, informed consent was
obtained from each participant. Asthma control was assessed using the asthma
control test (ACT), and a structured questionnaire was administered to
obtain information regarding lifestyle factors, including tobacco smoking,
alcohol drinking, physical exercise, and diet. Both bivariate and
multivariate analyses were conducted.

Results

The proportions of total control (ACT = 25), well controlled (ACT = 20-24),
and poorly controlled (ACT < 20) were 27.5%, 48.1%, and 24.5%,
respectively. The proportions of patients in the asthma treatment steps as
measured by Global Initiative for Asthma 2007 in step 1, step 2, step 3,
step 4, and step 5 were 5.5%, 17.4%, 7.6%, 60.2%, and 9.4%, respectively.
Body mass index, direct tobacco smoking status and alcohol drinking were not
associated with asthma control. On the other hand, younger age (< 65
years old), passive smoking, periodical exercise (> 3 metabolic
equivalents-h/week), and raw vegetable intake (> 5 units/week) were
significantly associated with good asthma control by bivariate analysis.
Younger age, periodical exercise, and raw vegetable intake were
significantly associated with good asthma control by multiple linear
regression analysis.

Conclusions

Periodical exercise and raw vegetable intake are associated with good asthma
control in Japanese patients.

Introduction

Bronchial asthma attacks are often observed in several situations, including allergen
inhalation, smoking, alcohol drinking, exercise, and the use of non-steroidal
anti-inflammatory drugs. To date, many investigators have reported relationships
between several lifestyle factors and asthma incidence [1–7]. Increasing body mass
index (BMI), passive smoking, and low income are risk factors for asthma incidence
[1–4]. Daily intake of fresh fruit or vegetables in infancy decreases the risk
of asthma occurrence [5]. Previous increased
intakes of saturated fatty acids, myristic and palmitic acids, and butter appear to
be related to the risk of current asthma in children [6]. More frequent consumption of fruit, vegetables, and fish was
associated with a lower lifetime prevalence of asthma, whereas higher burger
consumption was associated with higher lifetime asthma prevalence [8].

On the other hand, other studies have reported that there were no clear relationships
between dietary patterns and asthma incidence [9,10]. These previous reports
focused on the relationship between asthma incidence and past lifestyle factors
including diet, but there have been few reports concerning the relationship between
asthma control and daily lifestyle [11].
Moreover, inconsistent findings have been observed in the existing studies looking
at factors associated with asthma control. The avoidance of inhaled allergens or
tobacco smoke has been known to have favorable effects on asthma control. However,
González Barcala and colleagues reported that alcohol drinking did not affect asthma
control [12]. Similarly, Westermann and
colleagues also did not find the relationship between asthma control and periodic
exercise [13]. Moreover, it remains unclear
whether other lifestyle-related factors are also related to asthma control.
Therefore, a comprehensive study was conducted to examine the associations between
various lifestyle factors and asthma control in Japanese asthmatic patients.

Materials and Methods

Ethics Statement

This study was approved by the Institutional Review Board of the National Center
for Global Health and Medicine and a written informed consent was obtained from
each participant. This study was conducted according to the principles expressed
in the Declaration of Helsinki.

Study Design

The study subjects included 437 stable asthmatic patients recruited from the
outpatient clinic of the National Center for Global Health and Medicine, Tokyo,
Japan in 2009–2010. Eligible patients were aged over 20 years and had a clinical
diagnosis of asthma supported by one or more other characteristics: variability
in peak expiratory flow of more than 20%; the airway reversibility by inhaled β2
agonist; hyperresponsiveness of methacholine challenge; recurrent dyspnea
episode with wheezing. We excluded patients who could not fill in the
questionnaire, or who did not visit the clinic regularly, or who was diagnosed
as asthma within 3 months of the study entry.

Asthma control for the last four weeks was assessed using the asthma control test
(ACT). A structured questionnaire was administered to obtain information
regarding lifestyle factors, including tobacco smoking, alcohol drinking,
physical exercise, dietary intakes, pets, living space, cleaning habits,
occupation, medical expenses, and asthma diary record. The exercise was defined
as the total amount of walking (2 metabolic equivalents (METs)), light exercise
(2 METs), moderate exercise (4 METs), heavy exercise (6 METs), and gardening (2
METs). Concerning the dietary intakes, we collected information regarding the
consumption of cooked vegetables, raw vegetables, citrus fruits, other fruits,
vegetable and fruit mixed juice, vegetable juice, and 100% fruit juice. Raw
vegetables referred uncooked, unprocessed vegetables, which are usually organic
or wild vegetables. They include uncooked tomatoes, carrots and leafy greens.
The amount of intakes was assessed by the conversion of “unit”, which was
defined as the amount of food held on one hand.

Statistical analyses

We assessed characteristics of participants and their bivariate association with
asthma control levels using Pearson’s χ2 test or Fisher’s exact test
for categorical variables and Student t-test, Mann–Whitney U
test, or Kruskal-Wallis test for continuous variables. Additional analyses were
conducted, stratified by sex (male and female) and age groups (≤ 64 years and
> 64 years). A multiple linear regression model was then constructed to
examine the association between asthma control scores and lifestyle-related
factors. Two-sided p-values of < 0.05 were regarded as
statistically significant. Data analyses were performed with STATA version 11.0
(Lakeway Drive College Station, TX, USA) or SPSS statics version 17.0.0 (IBM
Japan, Tokyo, Japan).

Results

Patients' characteristics

The patients' characteristics are shown in Table 1. The mean age of the patients was 64 years, and the average
duration of asthma was 18 years. Sixty percent of the patients were atopic,
54.7% of patients were non-smokers, and current smokers accounted for only 6.6%.
The comorbidities of the patients included allergic rhinitis (49.5%), allergic
dermatitis (13.6%), sinusitis (29.0%), and chronic obstructive pulmonary disease
(COPD) (11.0%). Regarding types of treatment they received, 93.2% of patients
used inhaled corticosteroid (ICS), and 66.4% of patients used a long acting β2
agonist (LABA). The proportions of patients in the asthma treatment steps as
measured by Global Initiative for Asthma (GINA) 2007 in step 1, step 2, step 3,
step 4, and step 5 were 5.5%, 17.4%, 7.6%, 60.2%, and 9.4%, respectively. The
proportion of patients with total control (ACT = 25), well control (ACT =
20-24), and poor control (ACT < 20) were 27.5%, 48.1%, and 24.5%,
respectively (Table 1Figure 1). Fifty-five
percent of patients in step 5 were poorly controlled (Figure 1). Although the proportion of poorly
controlled patients increased gradually depending on the enhanced treatment
steps, a direct association between treatment steps and asthma control was not
observed.

Relationships between asthma control and smoking, drinking, and
exercise

Table 2 shows the comparisons of median
ACT scores by sex, age groups, BMI categories, smoking status, alcohol drinking
status, and exercise amounts. The median ACT score was significantly higher in
patients aged of 64 years or younger than in patients aged over 65 years (Table 2). More than 60% of patients aged
under 64 maintained an ACT score of 25 (total control) (data not shown). Median
ACT score was not significantly different among patients in non-smokers, past
smokers, and current smokers. However, median ACT score was significantly lower
in passive smokers compared to that in non-passive-smokers (p =
0.03). However, passive smoking was excluded by stepwise selection under the
multiple linear regression analysis (Table
3). The median ACT score was also not significantly different among
alcohol drinkers and non-drinkers.

Regarding exercise, the median ACT score was significantly higher among patients
who exercised more than 80 minutes per week compared to that among patients who
exercised 80 minutes per week or less (p = 0.006) (Table 2). In term of the amount of
exercise, the median ACT score was significantly higher among patients who
exercised more than 3 METs-h per week compared to that among patients who did 3
METs-h per week or less (p = 0.005). Multiple linear regression
analysis confirmed the significance of the bivariate analysis (Table 3).

The relation of asthma control to diet

The comparisons of median ACT scores in levels of various vegetable and fruit
intakes are shown in Table 4. The
median ACT score was significantly higher among patients who consumed more than
5 units of raw vegetables per week compared to that among patients consuming
five units or less of raw vegetables per week (p = 0.02).
However, additional analyses stratified by gender and age groups showed that
this association was found only in men (p = 0.001) and in
patients aged > 64 years (p = 0.005) (Table 5 and Table 6). Similarly, as shown in Table 7, the median ACT score was
significantly higher among patients who consumed > 1 unit of vegetable juice
per week compared to that in patients consuming 1 unit or less of vegetable
juice per week (p = 0.02), but only in patients aged 64 years
or younger. In multiple linear regression analysis, raw fresh vegetable intake
remained significantly associated with higher levels of asthma control
(p = 0.005) (Table
8).

Association between vegetable or fruit intake and the ACT score on
multiple linear regression.

Discussion

Several studies have previously reported the relationships between lifestyle factors
and asthma incidence [1–7]. However, few reports have focused on the relationships
between asthma control and lifestyle factors. A total of 437 asthmatic patients were
interviewed in our outpatient clinic, and the relationships between asthma control
and several lifestyle factors were investigated. The relationships of smoking or
alcohol drinking with asthma have already been reported in several articles. Radon
and colleagues reported that passive smoking was a risk factor for asthma occurrence
[3], while Bakirtas reported that passive
smoking and low income were risk factors for asthma incidence [4]. Similar results were observed in the present study; patients
who were exposed to passive smoking or who could not pay any medical expenses for
asthma treatment, had a tendency to poor asthma control (data partly shown).
Regarding lifestyle-related factors, González reported that alcohol drinking did not
affect asthma control [12]. Similar results
were obtained in the present study.

Lucas and colleagues insisted on the importance of physical activity on decreases in
asthma prevalence [14]. On the other hand,
Westermann found that there was no relationship between asthma control and periodic
exercise [13]. However, moderate exercise
(> 80 min/week) was found to be associated with good asthma control in the
present study. The Japanese government has recommended that 4 METs-h/week exercise
is required for the prevention of lifestyle-related diseases. In the present study,
patients with more than 3 METs-h/week exercise had good asthma control.

Comparisons of median ACT scores by various vegetable and fruit
intakes stratified by age groups.

Several empirical studies have investigated the effects of dietary intakes on asthma.
Frode reported that daily intakes of fresh fruit or vegetables in infancy decreased
the risk of asthma in school-age children [5].
Rodriguez found that increased intakes of saturated fatty acids, myristic and
palmitic acids, and butter appeared to be related to the risk of current asthma in
children [6]. Other reports mentioned that
intakes of α-linolenic acid and a low ratio of n-6:n-3 PUFA were associated with
decreased exhaled NO and improved asthma control [8]. Nagel reported that more frequent consumption of fruit, vegetables,
and fish was associated with a lower lifetime prevalence of asthma, whereas high
burger consumption was associated with higher lifetime asthma prevalence [9]. On the other hand, other investigators
reported that there were no clear relationships between dietary patterns and asthma
incidence [10,11].

These previous reports focused on the relationships between asthma incidence and
diet, while the present study examined the relationships between asthma control and
diet. Particularly fresh vegetable, but not heated vegetable, intakes were
associated with good asthma control in the present study. The possible explanations
for this relationship remain to be investigated. In general, flavonoids and related
polyphenolic compounds in vegetables are lost with heating. There is a report that
flavonoids and related polyphenolic compounds had significant anti-inflammatory
activity [15]. Recently, Wood reported the
importance of intakes of antioxidants in vegetables for asthma [16]. Further studies are required to elucidate
the relationship between flavonoids or antioxidants and asthma control.

In general, citrus fruits contain more amount of vitamin C than other fruits.
Previous reports indicated the relationship between consumption of citrus fruits and
incidence of asthma [17,18]. Furthermore, citrus fruits contain anti-inflammatory
effect [19]. However, we could not find the
relation between the consumption of citrus fruits and asthma control in our study.
Although citrus fruits are also included in fruit mixed juice and 100% fruit juice,
the relation between asthma control and fruit mixed juice or 100% fruit juice was
not observed. One of the possible reasons is the genotype of the patient because
citrus fruits may influence the sensitivity of the treatment of asthma [20].

Findings from this study are strengthened by the use of reliable and standardized
questionnaire to measure asthma control levels. Diez reported the relationships
between asthma control and several risk factors, including sex, race, BMI, smoking,
level of education, and habitual activity, in Spanish asthmatic patients [21]. They used the asthma control questionnaire
(ACQ) to evaluate asthma control. This questionnaire reflected asthma control for
the most recent week. In the present study, we used the ACT questionnaire, which
reflects longer term (recent one month) of asthma control than the ACQ. For this
reason, we believe that the ACT is better than the ACQ for evaluation of asthma
control when comparing lifestyle factors.

The statistical significance of the relation between asthma control and exercise or
raw vegetable diet intake was observed in our multiple linear regression analysis.
However, the adjusted R squared was 0.049, indicating that the correlation
coefficient was relatively weak. Interpretation of the results of our study should
be made with caution. Since this study was conducted by only one institution,
further multicenter studies are required for universalization of our results.

In conclusion, periodical exercise and raw vegetable intakes are associated with good
asthma control in Japanese patients.

Acknowledgments

We thank Satoru Ishii, Go Naka, Satoshi Hirano, Yuichiro Takeda, Atsuto Yoshizawa,
Masayuki Hojo and Hiroko Arioka for the inclusion of their patients in this
study.

Funding Statement

This work was supported by grants-in-aid from the Ministry of
Health and Welfare of Japan. The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the
manuscript.

References

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